From 1 October 2006 to 31 January 2007, 213 confirmed cases of measles occurred in the Barcelona Region, resulting from the importation of one case.

The imported case was a six-year-old girl of Eastern European origin. She presented on 28 August 2006* with a fever of 38 ºC, mild rash and enanthema (mucosal rash). Although the source of her infection could not be laboratory-confirmed, she had attended a family gathering in Italy with her mother, where, according to very limited available information, other guests may also have had measles. The girl’s mother also had measles-like symptoms during their stay in Italy. The girl had never been vaccinated against measles, and when the serology results were found to be positive for IgM antibodies against measles virus, the public health authorities were immediately notified of the case. Due to the difficulty to contact the girl’s family, who live in a caravan, measures to hold back the spread of the disease could not be implemented. In addition, it was impossible to gather more information on the epidemiological background and to implement active surveillance for more cases. Three close relatives of the first case also consulted medical services at the end of September with developing rash, but refused any confirmation procedures. They were cousins, living in Barcelona and two other towns at a short distance from Barcelona, and had gathered at a funeral in the last week of September. One of the three cousins had beginning coryza symptoms at the funeral.

Around that time, a second case was notified and confirmed. This was a 10-month-old unvaccinated girl with rash onset on 10 October. Although she stayed in the same neighbourhood as the index case, contact between them could not be established. Subsequently, more cases began to occur in indigenous children (born in Spain) and later on, by 5 November, more relatives of the index case living in another town in the northern Barcelona Region became ill. They could be contacted and confirmed as measles cases (Figure 1).

Figure 1. Date of measles rash onset, measles outbreak in Barcelona region, October 2006 – February 2007

The link between these cases in the Eastern European family and their cousins and the first indigenous cases was only possible through genotyping of the virus. The five cases related to the index family were infected with the same measles virus genotype as 10 cases belonging to three clusters of indigenous cases, genotype D4.

Case definition
A confirmed case of measles was defined either as a case that was laboratory confirmed (by detection of IgM type antibodies against measles virus, positive PCR, or culture from urine), or as a case that met the clinical case definition and was epidemiologically linked to a laboratory confirmed case, as detailed in [1].

The epidemic curve for the outbreak from September 2006 to the end of January 2007, with the number of confirmed measles cases by week of onset is shown in Figure 1. The age distribution of confirmed cases is shown in Figure 2. The median age of confirmed cases is 14 months (range two months to 50 years). The two-month-old child as well as their mother were both laboratory-confirmed cases.

Figure 2. Distribution of confirmed measles cases by age groups. Catalonia, October 2006-February 2007

From October 2006 to February 2007 there were 213 cases of measles (laboratory-confirmed or epidemiological linked to a laboratory-confirmed case) with 41 hospital admissions. Seventy are still under investigation and 42 have been excluded as cases.** The outbreak is still ongoing. To date, only 15 urine samples have been genotyped and classified as D4, coinciding with the genotype circulating in Italy during the summer of 2006 [2]. This genotype has been imported during the last two to three years from Romanian immigrants, but circulation of indigenous measles virus has been interrupted since 2000 [3]. Transmission of the virus has been identified in pre-school facilities, hospitals and family settings. Fourteen of the total 213 confirmed cases had received either one or two doses of MMR vaccine, according to their age. These cases will be studied thoroughly once the results of urine genotyping are available.

Outbreak control actions taken
In response to a suspected measles case, active surveillance was set up. Susceptible contacts from six months of age were vaccinated with a first dose of MMR, or a second dose, if they had previously received only one dose. Contacts not eligible for vaccination (<six months or pregnant women) were given non-specific immunoglobulin, and vaccination was recommended after five to six months.

All children aged nine to 15 months living in the Barcelona Region will be immunized until the outbreak ceases. A second dose will be administered, when the nine- to 12-month-old babies reach 15 months of age, and those aged 12 to 15 months receiving the vaccine will be considered as prime immunized. Parents have been alerted by means of individualized letters advising them to contact their vaccination center as soon as possible in order to immunize their child with MMR vaccine. As a result, 16 634 infants were vaccinated at 228 vaccination centres throughout the Barcelona Region between 11 and 30 January 2007, which corresponds to 56% of the population in the age group from nine to 15 months. In addition, MMR vaccination was recommended to all susceptible health care staff.

Discussion
As a result of the Measles Elimination Programme implemented in Catalonia in 1991, the incidence of measles infections fell to less than 1/100 000 inhabitants. The last indigenous case reported in Catalonia was registered in 2000. Since then, the region has been free of measles with the exception of a few cases due to importation and mainly in the unvaccinated adult population [3,4].

In 1981, the combined measles-mumps-rubella (MMR) vaccine at age 15 months was added to the vaccination schedule of Catalonia, and by 1988, a second dose of the MMR vaccine for boys and girls (up to then only girls received a second dose for rubella immunization at 11 to 12 years) was added to the list of routine vaccinations. Since 1999, the second dose of MMR is administered to children when they are 4 years old. These changes in vaccination strategy resulted in a great decline in the number of reported measles cases [5].

During the last five years, the incidence was less than 1/100 000, and all cases have been imported or secondary to importation [6]. According to the latest sero-epidemiological study carried out in 2002, the overall prevalence of anti-measles antibodies in Catalonia was 98% (95% CI, 98-99%), almost equal to that obtained in the 1996 study [99% (95% CI, 98-99 %) [7]. Coverage for MMR in 2005 was 99% for the first dose and 92% for the second dose in Catalonia, and 97% for first dose and 92% for second dose in the rest of Spain [8]. Outbreaks have occurred in recent years, the most important being in Almeria (2003) with 186 cases and in Madrid (2006) with 177 cases, both after the importation of a case from abroad and affecting mainly unvaccinated adult population. As in an outbreak in La Rioja in 2005-2006 [9], the proportion of cases we observed in children younger than 15 months is noteworthy, given that this is below the recommended age in Catalonia for the first dose of MMR. This will be followed up in detail.

In the past two years, several large outbreaks in Romania and the Ukraine were the source of measles outbreaks in a number of EU countries that had already achieved high levels of measles control (Estonia, Germany, Lithuania, Portugal, Poland, Italy and Spain) [10]. Therefore, in order to reach the goal set by the World Health Organisation to eliminate measles from the European Region by the year 2010 [11], strengthened surveillance and high vaccination coverage need to be maintained in countries with low incidence to keep virus spread restricted to isolated susceptible groups. Furthermore, great efforts need to be made to reduce the incidence, especially in those European countries with low vaccination coverage [12].

Acknowledgements
We thank the technicians of the Barcelona Region from the Servei Català de la Salut and the Institut Català de la Salut and all health professionals in hospitals, primary care and vaccination centres who have given such valuable task in the implementation of all outbreak control measures. We also want to that thank Centro Nacional de Microbiología at Majadahonda and Centro Nacional Epidemiología in Madrid for their collaboration.

* Erratum: The text in line 2 was changed to "She presented on 28 August 2006 with a fever of 38 ºC", rather than "on 26 September 2006" as stated in the original text.
** Erratum: The sentence: "Seventy are still under investigation and 42 have been discharged from hospital." was corrected and now reads: "Seventy are still under investigation and 42 have been excluded as cases."
These changes were made on 1 March 2007.